An ultrasensitive impedimetric glycan-based biosensor for reliable and selective detection of inactivated, but intact influenza viruses H3N2 was developed. Such glycan-based approach has a distinct advantage over antibody-based detection of influenza viruses since glycans are natural viral receptors with a possibility to selectively distinguish between potentially pathogenic influenza subtypes by the glycan-based biosensors. Build-up of the biosensor was carefully optimized with atomic force microscopy applied for visualization of the biosensor surface after binding of viruses with the topology of an individual viral particle H3N2 analyzed. The glycan biosensor could detect a glycan binding lectin with a limit of detection (LOD) of 5 aM. The biosensor was finally applied for analysis of influenza viruses H3N2 with LOD of 13 viral particles in 1 μl, what is the lowest LOD for analysis of influenza viral particles by the glycan-based device achieved so far. The biosensor could detect H3N2 viruses selectively with a sensitivity ratio of 30 over influenza viruses H7N7. The impedimetric biosensor presented here is the most sensitive glycan-based device for detection of influenza viruses and among the most sensitive antibody or aptamer based biosensor devices.

Department of Chemistry and Biochemistry Mendel University in Brno Zemedelska 1 613 00 Brno Czech Republic

Department of Glycobiotechnology Institute of Chemistry Slovak Academy of Sciences Dubravska cesta 9 845 38 Bratislava Slovakia

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Air GM. Curr Opin Virol. 2014;7:128–133. PubMed PMC

Alley WR, Mann BF, Novotny MV. Chem Rev. 2013;113:2668–2732. PubMed PMC

Amano Y, Cheng Q. Anal Bioanal Chem. 2005;381:156–164. PubMed

Arthur CM, Cummings RD, Stowell SR. Curr Opin Chem Biol. 2014;18:55–61. PubMed PMC

Bertok T, Šedivá A, Filip J, Ilcikova M, Kasak P, Velic D, Jane E, Mravcová M, Rovenský J, Kunzo P, Lobotka P, et al. Langmuir. 2015;31:7148–7157. PubMed PMC

Blixt O, Westerlind U. Curr Opin Chem Biol. 2014;18:62–69. PubMed

Bournazos S, Klein F, Pietzsch J, Seaman, Michael S, Nussenzweig, Michel C, Ravetch, Jeffrey V. Cell. 2014;158:1243–1253. PubMed PMC

Burton DR, Poignard P, Stanfield RL, Wilson IA. Science. 2012;337:183–186. PubMed PMC

Cecioni S, Imberty A, Vidal S. Chem Rev. 2015;115:525–561. PubMed

Charych D, Cheng Q, Reichert A, Kuziemko G, Stroh M, Nagy JO, Spevak W, Stevens RC. Chem Biol. 1996;3:113–120. PubMed

Charych DH, Nagy JO, Spevak W, Bednarski MD. Science. 1993;261:585–588. PubMed

Cheng MS, Toh C-S. Analyst. 2013;138:6219–6229. PubMed

Critchley P, Dimmock NJ. Biorg Med Chem. 2004;12:2773–2780. PubMed

Cummings RD, Pierce JM. Chem Biol. 2014;21:1–15. PubMed PMC

Dalziel M, Crispin M, Scanlan CN, Zitzmann N, Dwek RA. Science. 2014;343:37. doi: 10.1126/science.1235681. PubMed DOI

Davis JJ, Tkac J, Humphreys R, Buxton AT, Lee TA, Ko Ferrigno P. Anal Chem. 2009;81:3314–3320. PubMed

Davis JJ, Tkac J, Laurenson S, Ko Ferrigno P. Anal Chem. 2007;79:1089–1096. PubMed

de Graaf M, Fouchier RAM. EMBO J. 2014;33:823–841. PubMed PMC

Endo T, Ozawa S, Okuda N, Yanagida Y, Tanaka S, Hatsuzawa T. Sens Actuat B: Chem. 2010;148:269–276.

Fu Y, Callaway Z, Lum J, Wang R, Lin J, Li Y. Anal Chem. 2014;86:1965–1971. PubMed

Geissner A, Anish C, Seeberger PH. Curr Opin Chem Biol. 2014;18:38–45. PubMed

Gemeiner P, Mislovicova D, Tkac J, Svitel J, Patoprsty V, Hrabarova E, Kogan G, Kozar T. Biotechnol Adv. 2009;27:1–15. PubMed

Gopinath SCB, Awazu K, Fons P, Tominaga J, Kumar PKR. Anal Chem. 2009;81:4963–4970. PubMed

Gopinath SCB, Awazu K, Fujimaki M, Shimizu K, Shima T. PLoS One. 2013;8:e69121. PubMed PMC

Gopinath SCB, Tang TH, Chen Y, Citartan M, Tominaga J, Lakshmipriya T. Biosens Bioelectron. 2014;61:357–369. PubMed

Guo D, Zhuo M, Zhang X, Xu C, Jiang J, Gao F, Wan Q, Li Q, Wang T. Anal Chim Acta. 2013;773:83–88. PubMed

Hidari K, Shimada S, Suzuki Y, Suzuki T. Glycoconjugate J. 2007;24:583–590. PubMed

Hsieh K, Ferguson BS, Eisenstein M, Plaxco KW, Soh HT. Acc Chem Res. 2015;48:911–920. PubMed

Hushegyi A, Bertok T, Damborsky P, Katrlik J, Tkac J. Chem Commun. 2015;51:7474–7477. PubMed PMC

Hushegyi A, Tkac J. Anal Methods. 2014;6:6610–6620. PubMed PMC

Jiang Y, Tan CY, Tan SY, Wong MSF, Chen YF, Zhang L, Yao K, Gan SKE, Verma C, Tan Y-J. Sens Actuat B: Chem. 2015;209:78–84.

Kiilerich-Pedersen K, Daprà J, Cherré S, Rozlosnik N. Biosens Bioelectron. 2013;49:374–379. PubMed

Krejcova L, Hynek D, Adam V, Hubalek J, Kizek R. Int J Electrochem Sci. 2012;7:10779–10801.

Krejcova L, Hynek D, Michalek P, Milosavljevic V, Kopel P, Zitka O, Konecna M, Kynicky J, Adam V, Hubalek J, Kizek R, et al. Int J Electrochem Sci. 2014a;9:3440–3448.

Krejcova L, Nejdl L, Rodrigo MAM, Zurek M, Matousek M, Hynek D, Zitka O, Kopel P, Adam V, Kizek R. Biosens Bioelectron. 2014b;54:421–427. PubMed

Lahiri J, Isaacs L, Tien J, Whitesides GM. Anal Chem. 1999;71:777–790. PubMed

Laurent N, Voglmeir J, Flitsch SL. Chem Commun. 2008;37:4400–4412. PubMed

Lee C, Gaston MA, Weiss AA, Zhang P. Biosens Bioelectron. 2013;42:236–241. PubMed PMC

Li S. Atomic force microscopy study on the mechanics of influenza viruses and liposomes. Georg-August-Universität Göttingen; 2012.

Macauley MS, Arlian BM, Rillahan CD, Pang P-C, Bortell N, Marcondes MCG, Haslam SM, Dell A, Paulson JC. J Biol Chem. 2014;289:35149–35158. PubMed PMC

Marín MJ, Rashid A, Rejzek M, Fairhurst SA, Wharton SA, Martin SR, McCauley JW, Wileman T, Field RA, Russell DA, et al. Org Biomol Chem. 2013;11:7101–7107. PubMed

Medina RA, García-Sastre A. Nat Rev Microbiol. 2011;9:590–603. PubMed PMC

Nomura K-i, Gopinath SCB, Lakshmipriya T, Fukuda N, Wang X, Fujimaki M. Nat Commun. 2013;4:2855. PubMed

Paleček E, Tkáč J, Bartošík M, Bertók T, Ostatná V, Paleček J. Chem Rev. 2015;115:2045–2108. PubMed PMC

Park S, Gildersleeve JC, Blixt O, Shin I. Chem Soc Rev. 2013;42:4310–4326. PubMed PMC

Pihikova D, Belicky S, Kasak P, Bertok T, Tkac J. Analyst. 2016 doi: 10.1039/C1035AN02322J. PubMed DOI PMC

Pritchard LK, Spencer DIR, Royle L, Bonomelli C, Seabright GE, Behrens AJ, Kulp DW, Menis S, Krumm SA, Dunlop DC, Crispin DJ, et al. Nat Commun. 2015;6 doi: 10.1038/ncomms8479. PubMed DOI PMC

Reichardt NC, Martín-Lomas M, Penadés S. Chem Soc Rev. 2013;42:4358–4376. PubMed

Reichert A, Nagy JO, Spevak W, Charych D. J Am Chem Soc. 1995;117:829–830.

Rodrigo MAM, Zitka O, Krejcova L, Hynek D, Masarik M, Kynicky J, Heger Z, Adam V, Kizek R. Int J Electrochem Sci. 2014;9:3431–3439.

Rogowski A, Briggs JA, Mortimer JC, Tryfona T, Terrapon N, Lowe EC, Basle A, Morland C, Day AM, Zheng HJ, Rogers TE et al. Nat Commun. 2015;6 doi: 10.1038/ncomms8481. PubMed DOI PMC

Rouvinski A, Guardado-Calvo P, Barba-Spaeth G, Duquerroy S, Vaney MC, Kikuti CM, Navarro Sanchez ME, Dejnirattisai W, Wongwiwat W, Haouz A, Girard-Blanc C, et al. Nature. 2015;520:109–113. PubMed

Ruigrok RWH, Andree PJ, Hooft Van Huysduynen RAM, Mellema JE. J Gen Virol. 1984;65:799–802. PubMed

Sato T, Ishii M, Ohtake F, Nagata K, Terabayashi T, Kawanishi Y, Okahata Y. Glycoconjugate J. 1999;16:223–227. PubMed

Shen F, Wang J, Xu Z, Wu Y, Chen Q, Li X, Jie X, Li L, Yao M, Guo X, Zhu T, et al. Nano Lett. 2012;12:3722–3730. PubMed

Song X, Heimburg-Molinaro J, Smith DF, Cummings RD. Glycoconjugate J. 2015;32:465–473. PubMed PMC

Stencel-Baerenwald JE, Reiss K, Reiter DM, Stehle T, Dermody TS. Nat Rev Microbiol. 2014;12:739–749. PubMed PMC

Svarovsky SA, Joshi L. Anal Methods. 2014;6:3918–3936.

Varki A. Essentials of Glycobiology. Cold Spring Harbor Laboratory Press; Cold Spring Harbor, N.Y: 2009. PubMed

Wang RH, Li YB. Biosensors & Bioelectronics. 2013;42:148–155. PubMed

Wangchareansak T, Sangma C, Ngernmeesri P, Thitithanyanont A, Lieberzeit PA. Anal Bioanal Chem. 2013;405:6471–6478. PubMed

Watanabe T, Watanabe S, Maher EA, Neumann G, Kawaoka Y. Trends Microbiol. 2014;22:623–631. PubMed PMC

Wesener DA, Wangkanont K, McBride R, Song XZ, Kraft MB, Hodges HL, Zarling LC, Splain RA, Smith DF, Cummings RD, Paulson JC, et al. Nat Struct Mol Biol. 2015;22:603–610. PubMed PMC

Wicklein B, del Burgo MÁM, Yuste M, Carregal-Romero E, Llobera A, Darder M, Aranda P, Ortín J, del Real G, Fernández-Sánchez C, Ruiz-Hitzky E. Adv Funct Mater. 2013;23:254–262.

Wu Z, Zhou CH, Chen JJ, Xiong CC, Chen Z, Pang DW, Zhang ZL. Biosens Bioelectron. 2015;68:586–592. PubMed

Yang ZH, Zhuo Y, Yuan R, Chai YQ. Biosens Bioelectron. 2015;69:321–327. PubMed

Mixed Zwitterion-Based Self-Assembled Monolayer Interface for Impedimetric Glycomic Analyses of Human IgG Samples in an Array Format